Table of Contents
ISRN Pharmacology
Volume 2012 (2012), Article ID 276902, 10 pages
http://dx.doi.org/10.5402/2012/276902
Research Article

Neural Circuit in the Dorsal Raphe Nucleus Responsible for Cannabinoid-Mediated Increases in 5-HT Efflux in the Nucleus Accumbens of the Rat Brain

Charles E. Schmidt College of Medicine, Florida Atlantic University, Boca Raton, FL 33431, USA

Received 5 April 2012; Accepted 29 May 2012

Academic Editors: G. A. Gudelsky and D. K. Miller

Copyright © 2012 Rui Tao and Zhiyuan Ma. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. V. D. P. Soares, A. C. Campos, V. C. D. Bortoli, H. Zangrossi, F. S. Guimarães, and A. W. Zuardi, “Intra-dorsal periaqueductal gray administration of cannabidiol blocks panic-like response by activating 5-HT1A receptors,” Behavioural Brain Research, vol. 213, no. 2, pp. 225–229, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. T. V. Zanelati, C. Biojone, F. A. Moreira, F. S. Guimarães, and S. R. L. Joca, “Antidepressant-like effects of cannabidiol in mice: possible involvement of 5-HT1A receptors,” British Journal of Pharmacology, vol. 159, no. 1, pp. 122–128, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. E. Schlicker and M. Kathmann, “Modulation of transmitter release via presynaptic cannabinoid receptors,” Trends in Pharmacological Sciences, vol. 22, no. 11, pp. 565–572, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Pistis, A. L. Muntoni, G. Pillolla, and G. L. Gessa, “Cannabinoids inhibit excitatory inputs to neurons in the shell of the nucleus accumbens: an in vivo electrophysiological study,” European Journal of Neuroscience, vol. 15, no. 11, pp. 1795–1802, 2002. View at Publisher · View at Google Scholar · View at Scopus
  5. I. Wallmichrath and B. Szabo, “Analysis of the effect of cannabinoids on GABAergic neurotransmission in the substantia nigra pars reticulata,” Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 365, no. 4, pp. 326–334, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Haj-Dahmane and R. Y. Shen, “Endocannabinoids suppress excitatory synaptic transmission to dorsal raphe serotonin neurons through the activation of presynaptic CB1 receptors,” Journal of Pharmacology and Experimental Therapeutics, vol. 331, no. 1, pp. 186–196, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. E. Palazzo, V. de Novellis, S. Petrosino et al., “Neuropathic pain and the endocannabinoid system in the dorsal raphe: pharmacological treatment and interactions with the serotonergic system,” European Journal of Neuroscience, vol. 24, no. 7, pp. 2011–2020, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. F. R. Bambico, N. Katz, G. Debonnel, and G. Gobbi, “Cannabinoids elicit antidepressant-like behavior and activate serotonergic neurons through the medial prefrontal cortex,” Journal of Neuroscience, vol. 27, no. 43, pp. 11700–11711, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Häring, G. Marsicano, B. Lutz, and K. Monory, “Identification of the cannabinoid receptor type 1 in serotonergic cells of raphe nuclei in mice,” Neuroscience, vol. 146, no. 3, pp. 1212–1219, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. C. K. J. Lieben, H. W. M. Steinbusch, and A. Blokland, “5,7-DHT lesion of the dorsal raphe nuclei impairs object recognition but not affective behavior and corticosterone response to stressor in the rat,” Behavioural Brain Research, vol. 168, no. 2, pp. 197–207, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. C. A. Lowry, M. W. Hale, A. K. Evans et al., “Serotonergic systems, anxiety, and affective disorder: focus on the dorsomedial part of the dorsal raphe nucleus,” Annals of the New York Academy of Sciences, vol. 1148, pp. 86–94, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Kusljic, J. Brosda, T. R. Norman, and M. van den Buuse, “Brain serotonin depletion by lesions of the median raphe nucleus enhances the psychotomimetic action of phencyclidine, but not dizocilpine (MK-801), in rats,” Brain Research, vol. 1049, no. 2, pp. 217–226, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. W. Adams, S. Kusljic, and M. van den Buuse, “Serotonin depletion in the dorsal and ventral hippocampus: effects on locomotor hyperactivity, prepulse inhibition and learning and memory,” Neuropharmacology, vol. 55, no. 6, pp. 1048–1055, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Sharp, L. Boothman, J. Raley, and P. Quérée, “Important messages in the “post”: recent discoveries in 5-HT neurone feedback control,” Trends in Pharmacological Sciences, vol. 28, no. 12, pp. 629–636, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. R. Tao and S. B. Auerbach, “Differential effect of NMDA on extracellular serotonin in rat midbrain raphe and forebrain sites,” Journal of Neurochemistry, vol. 66, no. 3, pp. 1067–1075, 1996. View at Google Scholar · View at Scopus
  16. R. Tao, Z. Ma, and S. B. Auerbach, “Influence of AMPA/kainate receptors on extracellular 5-hydroxytryptamine in rat midbrain raphe and forebrain,” British Journal of Pharmacology, vol. 121, no. 8, pp. 1707–1715, 1997. View at Publisher · View at Google Scholar · View at Scopus
  17. R. Tao and S. B. Auerbach, “Influence of inhibitory and excitatory inputs on serotonin efflux differs in the dorsal and median raphe nuclei,” Brain Research, vol. 961, no. 1, pp. 109–120, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. R. Tao and S. B. Auerbach, “GABAergic and glutamatergic afferents in the dorsal raphe nucleus mediate morphine-induced increases in serotonin efflux in the rat central nervous system,” Journal of Pharmacology and Experimental Therapeutics, vol. 303, no. 2, pp. 704–710, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. G. Paxinos and C. Watson, Rat Brain Stereotaxic Coordinates, Academic Press, New York, NY, USA, 1998.
  20. Y. Qu, L. Arckens, F. Vandesande, and E. Vandenbussche, “Sampling extracellular aspartate, glutamate and γ-aminobutyric acid in striate cortex of awake cat by in vivo microdialysis: surgical and methodological aspects,” Brain Research, vol. 866, no. 1-2, pp. 116–127, 2000. View at Publisher · View at Google Scholar · View at Scopus
  21. R. Tao, Z. Ma, and S. B. Auerbach, “Differential effect of local infusion of serotonin reuptake inhibitors in the raphe versus forebrain and the role of depolarization-induced release in increased extracellular serotonin,” Journal of Pharmacology and Experimental Therapeutics, vol. 294, no. 2, pp. 571–579, 2000. View at Google Scholar · View at Scopus
  22. F. Chaperon, P. Soubrié, A. J. Puech, and M. H. Thiébot, “Involvement of central cannabinoid (CB1) receptors in the establishment of place conditioning in rats,” Psychopharmacology, vol. 135, no. 4, pp. 324–332, 1998. View at Publisher · View at Google Scholar · View at Scopus
  23. D. Moranta, S. Esteban, and J. A. García-Sevilla, “Differential effects of acute cannabinoid drug treatment, mediated by CB1 receptors, on the in vivo activity of tyrosine and tryptophan hydroxylase in the rat brain,” Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 369, no. 5, pp. 516–524, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. N. E. Kaminski, M. E. Abood, F. K. Kessler, B. R. Martin, and A. R. Schatz, “Identification of a functionally relevant cannabinoid receptor on mouse spleen cells that is involved in cannabinoid-mediated immune modulation,” Molecular Pharmacology, vol. 42, no. 5, pp. 736–742, 1992. View at Google Scholar · View at Scopus
  25. M. Rinaldi-Carmona, F. Barth, C. Congy et al., “SR147778 [5-(4-bromophenyl)-1-(2,4-dichlorophenyl)-4-ethyl-N-(1- piperidinyl)-1H-pyrazole-3-carboxamide], a new potent and selective antagonist of the CB1 cannabinoid receptor: Biochemical and pharmacological characterization,” Journal of Pharmacology and Experimental Therapeutics, vol. 310, no. 3, pp. 905–914, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. G. L. Gessa, S. Serra, G. Vacca, M. A. M. Carai, and G. Colombo, “Suppressing effect of the cannabinoid CB1 receptor antagonist, SR147778, on alcohol intake and motivational properties of alcohol in alcohol-preferring sP rats,” Alcohol and Alcoholism, vol. 40, no. 1, pp. 46–53, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Manzanares, J. Corchero, J. Romero, J. J. Fernández-Ruiz, J. A. Ramos, and J. A. Fuentes, “Pharmacological and biochemical interactions between opioids and cannabinoids,” Trends in Pharmacological Sciences, vol. 20, no. 7, pp. 287–294, 1999. View at Publisher · View at Google Scholar · View at Scopus
  28. D. Viganò, T. Rubino, and D. Parolaro, “Molecular and cellular basis of cannabinoid and opioid interactions,” Pharmacology Biochemistry and Behavior, vol. 81, no. 2, pp. 360–368, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. A. J. Tallett, J. E. Blundell, and R. J. Rodgers, “Endogenous opioids and cannabinoids: system interactions in the regulation of appetite, grooming and scratching,” Physiology and Behavior, vol. 94, no. 3, pp. 422–431, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. R. Tao and S. B. Auerbach, “Involvement of the dorsal raphe but not median raphe nucleus in morphine-induced increases in serotonin release in the rat forebrain,” Neuroscience, vol. 68, no. 2, pp. 553–561, 1995. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Vásquez, R. Navarro-Polanco, G. Hernández et al., “Cannabinoids and dopamine receptors' action on calcium current in rat neurons,” Canadian Journal of Neurological Sciences, vol. 32, no. 4, pp. 529–537, 2005. View at Google Scholar · View at Scopus
  32. V. A. Mitchell, H. Kawahara, and C. W. Vaughan, “Neurotensin inhibition of GABAergic transmission via mGluR-induced endocannabinoid signalling in rat periaqueductal grey,” Journal of Physiology, vol. 587, no. 11, pp. 2511–2520, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Y. Zhang, M. Xu, Q. L. Miao, M. M. Poo, and X. H. Zhang, “Endocannabinoid-dependent homeostatic regulation of inhibitory synapses by miniature excitatory synaptic activities,” Journal of Neuroscience, vol. 29, no. 42, pp. 13222–13231, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. R. J. McLaughlin and G. Gobbi, “Cannabinoids and emotionality: a neuroanatomical perspective,” The Journal of Neuroscience, vol. 204, pp. 134–144, 2012. View at Google Scholar
  35. G. Ferraro, M. E. Montalbano, P. Sardo, and V. La Grutta, “Lateral habenular influence on dorsal raphe neurons,” Brain Research Bulletin, vol. 41, no. 1, pp. 47–52, 1996. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Sano, K. Mishima, E. Koushi et al., “Δ9-Tetrahydrocannabinol-induced catalepsy-like immobilization is mediated by decreased 5-HT neurotransmission in the nucleus accumbens due to the action of glutamate-containing neurons,” Neuroscience, vol. 151, no. 2, pp. 320–328, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Nakazi, U. Bauer, T. Nickel, M. Kathmann, and E. Schlicker, “Inhibition of serotonin release in the mouse brain via presynaptic cannabinoid CB1 receptors,” Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 361, no. 1, pp. 19–24, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. N. Egashira, K. Mishima, S. Katsurabayashi et al., “Involvement of 5-hydroxytryptamine neuronal system in Δ9-tetrahydrocannabinol-induced impairment of spatial memory,” European Journal of Pharmacology, vol. 445, no. 3, pp. 221–229, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. G. Gobbi, F. R. Bambico, R. Mangieri et al., “Antidepressant-like activity and modulation of brain monoaminergic transmission by blockade of anandamide hydrolysis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 51, pp. 18620–18625, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. E. S. Levine and B. L. Jacobs, “Neurochemical afferents controlling the activity of serotonergic neurons in the dorsal raphe nucleus: microiontophoretic studies in the awake cat,” Journal of Neuroscience, vol. 12, no. 10, pp. 4037–4044, 1992. View at Google Scholar · View at Scopus
  41. A. Brancucci, N. Berretta, N. B. Mercuri, and W. Francesconi, “Presynaptic modulation of spontaneous inhibitory postsynaptic currents by gamma-hydroxybutyrate in the substantia nigra pars compacta,” Neuropsychopharmacology, vol. 29, no. 3, pp. 537–543, 2004. View at Publisher · View at Google Scholar · View at Scopus
  42. F. Jia, D. Chandra, G. E. Homanics, and N. L. Harrison, “Ethanol modulates synaptic and extrasynaptic GABAA receptors in the thalamus,” Journal of Pharmacology and Experimental Therapeutics, vol. 326, no. 2, pp. 475–482, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Adell, P. Celada, M. T. Abellán, and F. Artigas, “Origin and functional role of the extracellular serotonin in the midbrain raphe nuclei,” Brain Research Reviews, vol. 39, no. 2-3, pp. 154–180, 2002. View at Publisher · View at Google Scholar · View at Scopus
  44. R. McQuade and T. Sharp, “Functional mapping of dorsal and median raphe 5-hydroxytryptamine pathways in forebrain of the rat using microdialysis,” Journal of Neurochemistry, vol. 69, no. 2, pp. 791–796, 1997. View at Google Scholar · View at Scopus
  45. F. Bergquist, H. S. Niazi, and H. Nissbrandt, “Evidence for different exocytosis pathways in dendritic and terminal dopamine release in vivo,” Brain Research, vol. 950, no. 1-2, pp. 245–253, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Ludwig, N. Sabatier, P. M. Bull, R. Landgraf, G. Dayanithi, and G. Leng, “Intracellular calcium stores regulate activity-dependent neuropeptide release from dendrites,” Nature, vol. 418, no. 6893, pp. 85–89, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. D. Becquet, M. Faudon, and F. Hery, “The role of serotonin release and autoreceptors in the dorsalis raphe nucleus in the control of serotonin release in the cat caudate nucleus,” Neuroscience, vol. 39, no. 3, pp. 639–647, 1990. View at Publisher · View at Google Scholar · View at Scopus
  48. J. L. Lukkes, G. L. Forster, K. J. Renner, and C. H. Summers, “Corticotropin-releasing factor 1 and 2 receptors in the dorsal raphé differentially affect serotonin release in the nucleus accumbens,” European Journal of Pharmacology, vol. 578, no. 2-3, pp. 185–193, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. R. Tao and S. B. Auerbach, “Regulation of serotonin release by GABA and excitatory amino acids,” Journal of Psychopharmacology, vol. 14, no. 2, pp. 100–113, 2000. View at Google Scholar · View at Scopus
  50. Z. Ma, E. Pearson, and R. Tao, “CART peptides increase 5-hydroxytryptamine in the dorsal raphe and nucleus accumbens of freely behaving rats,” Neuroscience Letters, vol. 417, no. 3, pp. 303–307, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Mendiguren and J. Pineda, “Effect of the CB1 receptor antagonists rimonabant and AM251 on the firing rate of dorsal raphe nucleus neurons in rat brain slices,” British Journal of Pharmacology, vol. 158, no. 6, pp. 1579–1587, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. P. K. Y. Chan and W. H. Yung, “Occlusion of the presynaptic action of cannabinoids in rat substantia nigra pars reticulata by cadmium,” Neuroscience Letters, vol. 249, no. 1, pp. 57–60, 1998. View at Publisher · View at Google Scholar · View at Scopus
  53. N. Hájos, I. Katona, S. S. Naiem et al., “Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations,” European Journal of Neuroscience, vol. 12, no. 9, pp. 3239–3249, 2000. View at Publisher · View at Google Scholar · View at Scopus
  54. L. Ferraro, M. C. Tomasini, T. Cassano et al., “Cannabinoid receptor agonist WIN 55,212-2 inhibits rat cortical dialysate γ-aminobutyric acid levels,” Journal of Neuroscience Research, vol. 66, no. 2, pp. 298–302, 2001. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Caillé and L. H. Parsons, “Cannabinoid modulation of opiate reinforcement through the ventral striatopallidal pathway,” Neuropsychopharmacology, vol. 31, no. 4, pp. 804–813, 2006. View at Publisher · View at Google Scholar · View at Scopus